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Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults
Open accessAbstract
Oxytocin receptors (OXTR) in the nucleus accumbens (NAcc) promote alloparental behavior and partner preference formation in female prairie voles. Within the NAcc there is significant individual variation in OXTR binding and virgin juvenile and adult females with a high density of OXTR in the NAcc display an elevated propensity to engage in alloparental behavior toward novel pups. Over-expression of OXTR in the NAcc of adult female prairie voles using viral vector gene transfer facilitates partner preference formation, but has no effect on alloparental behavior, even though OXTR antagonists infused into the NAcc blocks both behaviors. We therefore hypothesized that long-term increases in OXTR signaling during development may underlie the relationship between adult OXTR density in the NAcc and alloparental behavior. To test this hypothesis, we used viral vector gene transfer to increase OXTR density in the NAcc of prepubertal, 21day old female prairie voles and tested for both alloparental behavior and partner preference formation as adults. Consistent with a developmental impact of OXTR signaling, adults over-expressing OXTR from weaning display both increased alloparental behavior and partner preference formation. Thus, the relatively acute impact of elevated OXTR signaling in the NAcc on partner preference formation previously reported appears to be dissociable from the effects of longer term, developmentally relevant OXTR signaling necessary for modulating alloparental behavior. These results are consistent with the hypothesis that oxytocin can have both long-term "organizational" effects as well as acute "activational" effects on affiliative behaviors.
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In the citing paper
“Additionally, viral knockdown of OXTRs within the NAc of voles disrupts partner preference formation and alloparental behavior; however, pair bonding and maternal care are facilitated when OXTR expression in the NAc is increased, suggesting a direct role of NAc OXTRs in driving affiliative behavior [15,140].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [140]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Prairie voles are highly nurturing, and virgin females can display spontaneous levels of maternal care depending on density of nucleus accumbens oxytocin receptors”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Keebaugh & Young 2011
In the citing paper
“Increasing OXTR density in the NAcc using viral-vector mediated gene transfer facilitates partner preference formation, while decreasing OXTR density in the same region using RNA interference inhibits such bonding (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
In the citing paper
“Increasing OXTR density in the NAcc using viral-vector mediated gene transfer facilitates partner preference formation, while decreasing OXTR density in the same region using RNA interference inhibits such bonding (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
In the citing paper
“and OXTR variation mediates individual differences in pair bonding behaviors (37–39).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [37]
In the citing paper
“Additionally, in prairie voles, the expression of spontaneous maternal behavior in virgin females is organized by developmental (and not adult) levels of OTR in the NAC shell, and is prevented by OTR antagonist injected into this region (Olazabal and Young 2006a; Ross et al 2009b; Keebaugh and Young 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Keebaugh and Young 2011
In the citing paper
“several studies have characterized the role of intra-NAc OR activation in facilitating partner preference formation in female, but not male, prairie voles”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Keebaugh and Young 2011
In the citing paper
“Viral-mediated small interfering RNA knockdown of OXTR in NAcc of prairie voles inhibits partner preference (138), while overexpressing NAcc OXTR enhances partner preference formation (139).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [139]
In the citing paper
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [29]
In the citing paper
“Furthermore, OXTR signaling in the NAc plays a critical role for the formation of a preference for an individual, and the density of NAc OXTR correlates with such preferences 27–29.”
From Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles (2022) · cites this paper as [29]
In the citing paper
“experimentally increasing9 or decreasing10 OXTR expression in the prairie vole nucleus accumbens modulated partner preference behavior”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
In the citing paper
“animal models demonstrating that OXTR expression levels directly modulate social behavior9,10”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
In the citing paper
“and that increased OXTR gene expression is associated with increased oxytocin binding”
From Oxytocin pathway gene networks in the human brain (2019) · cites this paper as [9]
In the citing paper
“By injecting an adeno-associated viral vector into the nucleus accumbens (NAcc) shell of female prairie voles at PND21 they were able to facilitate alloparental care, as measured by reductions in approach times and increases in time spent licking and grooming pups compared to controls (57).”
From Oxytocin during Development: Possible Organizational Effects on Behavior (2015) · cites this paper as [57]
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Kaplan, H. S., Horvath, P. M., Rahman, M. M., & Dulac, C. G. (2024) · Physiological Reviews · doi:10.1152/physrev.00036.2023 · Cited by 20
Hiura, L. C., & Ophir, A. G. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12338 · Cited by 19
Harder, H. J., Searles, C. T., Vogt, M. E., & Murphy, A. Z. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105384 · Cited by 16
Oxytocin receptors in the nucleus accumbens shell are necessary for the onset of maternal behavior
Witchey, S. K., Haupt, A., & Caldwell, H. K. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1356448 · Cited by 16
Fu, Y., & Depue, R. A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.026 · Cited by 18
Morales, L. K. N., Boender, A. J., Young, L. J., Lamprea, M. R., & Smith, A. S. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1409316 · Cited by 13
Taylor, J. H., Intorre, A. A., & French, J. A. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00181 · Cited by 16
Sex differences of oxytocin and vasopressin in social behaviors
Lu, Q., & Hu, S. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820107-7.00005-7 · Cited by 19
On the origins of diversity in social behavior
YOUNG, L. J., & ZHANG, Q. (2021) · Japanese Journal of Animal Psychology · doi:10.2502/janip.71.1.4 · Cited by 13
Borland, J. M. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101175 · Cited by 13
Mate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12
The Role of Early Life Experience and Species Differences in Alcohol Intake in Microtine Rodents
Anacker, A. M. J., Ahern, T. H., Young, L. J., & Ryabinin, A. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039753 · Cited by 13
Keebaugh, A. C., Modi, M. E., Barrett, C., Jin, C., & Young, L. J. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-54 · Cited by 12
Quintana, D. S. (2018) · OSF Preprints (OSF Preprints) · Cited by 12
The neural circuits of monogamous behavior
López-Gutiérrez, M. F., Mejía-Chávez, S., Alcauter, S., & Portillo, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.978344 · Cited by 12
The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
Donaldson, Z. R., & Young, L. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_4 · Cited by 12
Paiva, L., Sabatier, N., Leng, G., & Ludwig, M. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12454 · Cited by 12
Quintana, D. S., Rokicki, J., van der Meer, D., Alnæs, D., Kaufmann, T., Córdova‐Palomera, A., Dieset, I., Andreassen, O. A., & Westlye, L. T. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/149526 · Cited by 12
Taylor, J. H., & Grieb, Z. A. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.100996 · Cited by 10
Association between parental behaviors and structural plasticity in the brain of male rodents
Inada, K., & Miyamichi, K. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.06.007 · Cited by 9
Rethinking the Architecture of Attachment: New Insights into the Role for Oxytocin Signaling
Berendzen, K. M., & Manoli, D. S. (2022) · Affective Science · doi:10.1007/s42761-022-00142-5 · Cited by 9
Tsukamoto, M., Nagai, L. A., Inoue, K., Kandasamy, L. C., Pires, M. F., Shin, M., Nagasawa, Y., Sambuu, T., Nakai, K., Itohara, S., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.01.518660 · Cited by 9
Loth, M. K., Schmidt, J. C., Gonzalez, C. A., Brusman, L. E., Sadino, J. M., Winther, K. E., Protter, D. S. W., & Donaldson, Z. R. (2025) · Scientific Reports · doi:10.1038/s41598-025-06367-1 · Cited by 8
Wu, R., Song, Z., & Tai, F. (2018) · Journal of Comparative Physiology A · doi:10.1007/s00359-018-1262-4 · Cited by 6
Fricker, B. A., Boender, A. J., Young, L. J., & Kelly, A. M. (2025) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2025.107496 · Cited by 5
Perkeybile, A. M., Kenkel, W. M., Yee, J. R., Waugh, R. E., Lillard, T. S., Ferris, C. F., Carter, C. S., & Connelly, J. J. (2025) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-025-07868-7 · Cited by 4
Municchi, D., Mancini, C., Nutarelli, S., Tiberi, M., D’Addario, S. L., Chila, G., Passeri, A., Massa, G., Segni, M. D., Babicola, L., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03437-8 · Cited by 4
Metadata
- Authors
- Keebaugh, A. C., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Keebaugh, Alaine C.
- ORCID
- Young, Larry J.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2011-11
- Volume
- 60
- Issue
- 5
- Pages
- 498-504
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC3210320
- OpenAlex
- W1969779840
- Cited by
- 154
- References
- 48
- Citations by year
- 2026: 3 · 2025: 12 · 2024: 9 · 2023: 11 · 2022: 10 · 2021: 10 · 2020: 23 · 2019: 7 · 2018: 17 · 2017: 7 · 2016: 10 · 2015: 12 · 2014: 6 · 2013: 11 · 2012: 5
- FWCI
- 10.01
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (MH064692, RR00165)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Human-Animal Interaction Studies
- Keywords
- oxytocin receptor, nucleus accumbens, Microtus ochrogaster, mate preferences, prepubertal development, oxytocin, organizational effects, activational effects, affiliative behavior, female social behavior, gene overexpression
- MeSH terms
- Animals, Arvicolinae, Female, Nucleus Accumbens, Pair Bond, Receptors, Oxytocin
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